Corbett-Detig Russell B, Hartl Daniel L, Sackton Timothy B
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge Massachusetts, United States of America; Department of Integrative Biology, University of California, Berkeley, Berkeley, California, United States of America.
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge Massachusetts, United States of America.
PLoS Biol. 2015 Apr 10;13(4):e1002112. doi: 10.1371/journal.pbio.1002112. eCollection 2015 Apr.
The neutral theory of molecular evolution predicts that the amount of neutral polymorphisms within a species will increase proportionally with the census population size (Nc). However, this prediction has not been borne out in practice: while the range of Nc spans many orders of magnitude, levels of genetic diversity within species fall in a comparatively narrow range. Although theoretical arguments have invoked the increased efficacy of natural selection in larger populations to explain this discrepancy, few direct empirical tests of this hypothesis have been conducted. In this work, we provide a direct test of this hypothesis using population genomic data from a wide range of taxonomically diverse species. To do this, we relied on the fact that the impact of natural selection on linked neutral diversity depends on the local recombinational environment. In regions of relatively low recombination, selected variants affect more neutral sites through linkage, and the resulting correlation between recombination and polymorphism allows a quantitative assessment of the magnitude of the impact of selection on linked neutral diversity. By comparing whole genome polymorphism data and genetic maps using a coalescent modeling framework, we estimate the degree to which natural selection reduces linked neutral diversity for 40 species of obligately sexual eukaryotes. We then show that the magnitude of the impact of natural selection is positively correlated with Nc, based on body size and species range as proxies for census population size. These results demonstrate that natural selection removes more variation at linked neutral sites in species with large Nc than those with small Nc and provides direct empirical evidence that natural selection constrains levels of neutral genetic diversity across many species. This implies that natural selection may provide an explanation for this longstanding paradox of population genetics.
分子进化的中性理论预测，一个物种内中性多态性的数量将与普查种群大小（Nc）成比例增加。然而，这一预测在实践中并未得到证实：虽然Nc的范围跨越多个数量级，但物种内的遗传多样性水平却落在一个相对较窄的范围内。尽管理论上的观点援引了大种群中自然选择效率的提高来解释这种差异，但对这一假设的直接实证检验却很少。在这项工作中，我们使用来自广泛分类学上不同物种的群体基因组数据对这一假设进行了直接检验。为此，我们依据的事实是，自然选择对连锁中性多样性的影响取决于局部重组环境。在重组相对较低的区域，被选择的变异通过连锁影响更多的中性位点，重组与多态性之间的相关性使得我们能够对选择对连锁中性多样性的影响程度进行定量评估。通过使用合并模型框架比较全基因组多态性数据和遗传图谱，我们估计了40种专性有性真核生物中自然选择降低连锁中性多样性的程度。然后，我们以体型和物种范围作为普查种群大小的代理指标，表明自然选择的影响程度与Nc呈正相关。这些结果表明，自然选择在Nc大的物种中比在Nc小的物种中消除了更多连锁中性位点上的变异，并提供了直接的实证证据，证明自然选择在许多物种中限制了中性遗传多样性水平。这意味着自然选择可能为群体遗传学中这个长期存在的悖论提供一种解释。
